Concentrations of organochlorine pesticides in umbilical cord blood and related lifestyle and dietary intake factors among pregnant women of the Huaihe River Basin in China

Environment International 92–93 (2016) 276–283

Contents lists available at ScienceDirect

Environment International journal homepage: www.elsevier.com/locate/envint

Concentrations of organochlorine pesticides in umbilical cord blood and related lifestyle and dietary intake factors among pregnant women of the Huaihe River Basin in China Dan Luo a, Yabing Pu a, Haoyuan Tian b, Juan Cheng a, Tingting Zhou a, Yun Tao a, Jing Yuan a, Xin Sun b,⁎, Surong Mei a,⁎ a Key Laboratory of Environment and Health, Ministry of Education & Ministry of Environmental Protection, and State Key Laboratory of Environment Health (Incubation), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, #13 Hangkong Road, Wuhan, Hubei, 430030, China b Key Laboratory of Chemical Safety and Health, National Institute of Occupational Health and Poison Control, Chinese Center for Disease Control and Prevention, #27 Nan Wei Road, West City District, Beijing 100050, China

a r t i c l e

i n f o

Article history: Received 20 November 2015 Received in revised form 6 April 2016 Accepted 13 April 2016 Available online xxxx Keywords: Organochlorine pesticides Pregnant women Lifestyle factors Dietary intake Umbilical cord blood Huaihe River Basin

a b s t r a c t Organochlorine pesticides (OCPs), one of the persistent organic pollutants (POPs) with highly lipophilic properties, long half-lives, and persistence in the environment, are prevalent in the environment even though they have been banned for N 30 years. We aimed to investigate the current OCP exposure levels in cord blood from healthy pregnant women residing in the Huaihe River Basin, China, and examined the association between OCP levels and dietary habits and lifestyle factors. In this study, we measured the exposure levels of 17 OCPs in the umbilical cord blood from 999 healthy pregnant women; we also administered 1000 self-reported questionnaires regarding the general characteristics and dietary habits of those women. Our results showed that ρ,ρ′-DDE, ρ,ρ′-DDT, aldrin, dieldrin, and methoxychlor, which had higher measured concentrations (2.01 ± 1.89, 4.31 ± 5.68, 7.29 ± 8.74, 5.27 ± 7.65, and 0.98 ± 1.42 ng/mL, respectively) and detection frequencies (99.69%, 100.00%, 81.79%, 75.00%, and 74.49%, respectively), were the predominant OCPs in cord blood, and the higher levels of DDTs, aldrin, dieldrin, and methoxychlor were mainly due to recent use. In addition, most of the HCHs in cord blood were derived not only from historical use of technical HCH, but also from the additional use of lindane. In addition, we found that the education level of the pregnant women and monthly household income were positively correlated with OCP levels, particularly ρ,ρ′-DDE, aldrin, and dieldrin. Furthermore, the consumption of red meat (pork, beef, and lamb), fish, and bean products may be an important contributing factor to the increased concentrations of OCPs in cord blood, while the intake of poultry and pickles was negatively correlated with aldrin level. This study is the first to provide adequate data on current OCP exposure levels in cord blood from pregnant women in the Huaihe River Basin. © 2016 Elsevier Ltd. All rights reserved.

1. Introduction As important insecticides, organochlorine pesticides (OCPs) have been mass produced and widely applied in agriculture worldwide since the 1940s. Due to its effectiveness in controlling mosquitoes, OCPs have been extensively used in the prevention of malaria and typhoid fever, and great progress has been made in this regard. However, Abbreviations: OCPs, organochlorine pesticides; POPs, persistent organic pollutants; HCH, hexachlorcyclohexane; DDT, dichlorodiphenyltrichloroethane; HCB, hexachlorobenzene; DCM, dichloromethane; SIM, selective ion monitoring; LOD, limit of detection; LOQ, limit of quantitation; RSDs, relative standard deviations; SD, standard deviation; ND, not detection; NA, data are not available. ⁎ Corresponding authors. E-mail addresses: [email protected] (X. Sun), [email protected] (S. Mei).

http://dx.doi.org/10.1016/j.envint.2016.04.017 0160-4120/© 2016 Elsevier Ltd. All rights reserved.

concerns emerged regarding the application of OCPs as increasing evidence of their adverse health effects has been uncovered. Relevant studies have suggested a link between the exposure to OCPs in humans and a wide range of adverse health effects, including endocrine disorders or reproductive-related effects (Bretveld et al., 2006; Li et al., 2008; Nicolopoulou-Stamati and Pitsos, 2001; Safea, 2004; Toft et al., 2004), immune dysfunction (Nagayama et al., 2007; Noakes et al., 2006), nervous system injury (Kamel and Hoppin, 2004; Keifer and Firestone, 2007; Ren et al., 2011), and cancer or tumors (McGlynn et al., 2006; Weiderpass et al., 2000; Wolff et al., 2000; Xu et al., 2010). Moreover, since OCPs possess the ability to transfer from mother to fetus through placental transport (Saxena et al., 1981a), there is evidence that prenatal OCP exposure causes adverse birth outcomes such as low birth weight (Dewan et al., 2013; Eggesbø et al., 2009), preterm labor

D. Luo et al. / Environment International 92–93 (2016) 276–283

(Pathak et al., 2009), spontaneous abortions (Korrick et al., 2001; Saxena et al., 1981b), decreased crown-heel length (Dewan et al., 2013; Eskenazi et al., 2004), smaller birth size (Dewan et al., 2013; Lopez-Espinosa et al., 2011; Sagiv et al., 2007), and developmental disorders (Eskenazi et al., 2006). As typical persistent organic pollutants (POPs), OCP properties such as persistence in the environment, long half-lives, and high lipophilicity have enabled them to bioaccumulate in human adipose tissue through the food chain and stay stable inside the human body for a long time (Clarkson, 1995; Shen et al., 2005; Sheng et al., 2013). Therefore, the production and use of some OCPs have been banned or restricted according to the Stockholm Convention on persistent organic pollutants (POPs) (No, 2005), including aldrin, dieldrin, endrin, heptachlor, and dichlorodiphenyltrichloroethane (DDT). Hexachlorocyclohexane (HCH) is an exception since it has been permitted to a unintentional production. As the leading agricultural country in the world, China had a largescale production and consumption of OCPs before the 1980s, especially DDTs and HCHs. Although the production and use of OCPs for agriculture had been banned in China since 1983, DDT was still used for dicofol production, and HCB, mirex, and chlordane were used for other reasons (Guo et al., 2014). Recent studies on OCP distribution have caused researchers to revisit previous concerns. It was found that OCPs could be detected not only in soil, water, air, sediment, foods, vegetables, fish, and poultry, but also in the blood, adipose tissue, and breast milk of the general population in China (Fang et al., 2007; Nakata et al., 2002; Nakata et al., 2005; Poon et al., 2005; Qiu et al., 2004; Tao et al., 2009; Yang et al., 2006; Yang et al., 2005; Zhou et al., 2006). The Huaihe River Basin, one of the most populated areas in East China, has been reported to suffer environmental problems, including OCP residues (Hong et al., 2006; Wang et al., 2006). Even though the Chinese government made a great effort to control the pollution in the Huaihe River, serious environmental problems still existed. Recent studies have revealed that residual OCPs are present in sediments and surface water in the upper reach of the Huaihe River (Feng et al., 2011; Sun et al., 2010). The presence of OCPs in sediments and surface water is a result of biological accumulation of multiple residues via the food chain and a threat to human health. However, so far there appears to be little or no available information regarding current OCP exposure levels among the general population in the Huaihe River Basin, thus the specific OCP hazards to individuals remain unclear. This study was conducted to investigate current OCP exposure levels in cord blood from pregnant women in the Huaihe River Basin. Since dietary and lifestyle-related risk factors had been found to be the main route for exposure to OCPs for the non-occupational population (Cao et al., 2011; Lee et al., 2007; Mariscal-Arcas et al., 2010), associations between related factors and the concentration of OCPs in individuals were also taken into account in this study. We hope this study will help identify current OCP exposure levels of individuals in the Huaihe River Basin and provide basic data for OCP management. 2. Methods and materials 2.1. Study design and cord blood sample collection The study was conducted between November 2013 and June 2014, and a total of 1000 pregnant women were enrolled from the local hospital of the Huaihe River Basin. Responses to 1000 questionnaires were obtained, and 999 umbilical cord blood samples were collected. None the participants had been occupationally exposed to OCPs. Women with chronic illnesses (diabetes; renal, cardiovascular, hepatobiliary, thyroid-related, and pulmonary diseases; HIV; etc.) and pregnancy complications (pregnancy-induced hypertension, urinary tract infection, etc.) were excluded. Before umbilical cord blood was obtained, the pregnant women were required to sign a consent form after receiving a detailed explanation of the study. Participants provided details regarding age, education

277

level, monthly household income, smoking habits, alcoholic beverage consumption, length of residency, parity, history of disease, and dietary habits through a questionnaire. The dietary information during the period of gestation was gathered from the food frequency questionnaire (FFQ). The diet items of the FFQ included staple foods (rice, steamed bread, noodles, corn), red meat (pork, beef, lamb), poultry (chicken, duck, goose), fish, seafood (shrimp, shellfish, sea cucumbers, crab), fruit, bean products, milk, yogurt, eggs, dry fruits, tubers (potato, sweet potato), vegetables, pickles, and tea. The responses of dietary intake habits were divided into the following categories: never or less than once a month, 1–3 times/month, 1–6 times/week, and ≥ 1 time/ day. All mothers were surveyed by a trained interviewer. Approximately 10 mL of umbilical cord blood was collected in EDTA vials at the time of delivery, and the centrifuged plasma samples were stored at − 80 °C before use. This study was reviewed and approved by the Ethics Committee of the National Institute for Occupational Health and Poison Control, Chinese Center for Disease Control and Prevention. 2.2. Chemical analysis A pesticide mixture standard (Pesticide Mix 17, Sigma-Aldrich, St. Louis, MO, USA) contained α-HCH, β-HCH, ϒ-HCH (lindane), δ-HCH, heptachlor, aldrin, heptachlor epoxide, endosulfan I, ρ,ρ′-DDE, dieldrin, endrin, endosulfan II, ρ,ρ′-DDD, endrin aldehyde, endosulfan sulfate, ρ,ρ′DDT, and methoxychlor at 2 mg/mL per component in hexane:toluene (1:1), and was purchased from Sigma-Aldrich. 13C6-labelled HCB (hexachlorobenzene) was used as the internal standard and was purchased from Sigma-Aldrich; the urea (analytical reagent) was purchased from Sinopharm Chemical Reagent Co., Ltd. (Shanghai, China); the methanol was of HPLC grade purity and was purchased from Merck KgaA (Darmstadt, Germany); and the hexane and dichloromethane (DCM) (pesticide grade) were purchased from Sigma-Aldrich. The procedure for sample preparation and measurement of OCPs from the plasma sample was carried out as described previously (Sundberg et al., 2006) with minor modifications. Briefly, thawed and homogenized plasma samples (0.5 mL) were spiked with 13C6-labelled HCB and then vortexed after adding 0.5 mL of deionized water. Before extraction, the plasma proteins were denatured with 500 mg of urea, followed by vortex and sonication for 25 min. Solid phase extraction of the samples was performed on an Oasis® HLB extraction cartridge (3 cm3/60 mg) (Waters Corporation, Milford, MA, USA) and mounted in Vac Elut SPE 24 (Agilent Technologies, Palo Alto,CA, USA). Before loading the plasma samples, the HLB cartridges were cleaned and conditioned with 3 mL of DCM, 5 mL of methanol, and 5 mL of deionized water successively. The diluted plasma sample passed through the HLB cartridge by gravity flow and was rinsed twice with 1 mL of deionized water. The HLB cartridge was then washed with 5 mL of deionized water and a vacuum condition was applied for 1 h to remove residual water. The OCPs were then eluted with 5 mL of elution mixture (dichloromethane and n-hexane 1:9; v/v), and the pooled eluate was evaporated to near dryness under a stream of nitrogen. The extract was dissolved in 100 μL of hexane for further analysis. The analysis was performed on an Agilent 6890 N gas chromatography/5975B mass spectrometry system (Agilent Technologies, Palo Alto,CA, USA). High-purity helium (N99.999%) was used as a carrier gas at a constant flow of 1.0 mL min−1. The injector temperature was set at 250 °C, and the injection volume was 1 μL with the splitless mode. The extract separation was performed on a DB-5 ms capillary column (30 m × 0.25 mm × 0.25 μm). The oven temperature program was as follows: initial temperature 60 °C for 1 min, 30 °C min−1 to 180 °C held for 1 min, and then 7 °C min−1 to 280 °C held for 2 min. The mass spectrometer was operated in selective ion monitoring (SIM) mode and the electron ionization voltage was 70 eV. Temperatures of the transfer line, ionization source, and quadruples were 280 °C, 230 °C, and 150 °C, respectively. A solvent delay was set at 6 min.

278

D. Luo et al. / Environment International 92–93 (2016) 276–283

MassHunter software (Agilent Technologies) was used for instrumental control, data acquisition, and analysis. 2.3. Quality assurance and quality control Quantification of the targeted compounds was performed by the internal standard addition method with isotope-labelled OCPs. With each batch of 20 samples analyzed, quality control plasma samples and method blank samples were included in this study. Each sample was measured in duplicate. The calibration curves were from a range of 1.0–200 ng/mL for each analyte with R2 greater than 0.996. The limit of detection (LOD) and the limit of quantitation (LOQ)of the targeted compounds were defined as 3 times the ratio of signal-to-noise (S/ N = 3) and 10 times the ratio of S/N (S/N = 10). The corresponding LOD and LOQ were 0.08 to 2.31 ng/mL and 0.26 to 7.69 ng/mL. The recoveries of all compounds ranged from 72.0% to 119.0% with relative standard deviations (RSDs) of 1.0%–21.7% in plasma samples spiked at 20 and 100 ng/mL. 2.4. Statistical analyses In all statistical analyses, concentrations below the LOD were set at half of the LOD. The concentrations of all compounds were expressed as nanogram per milliliter (ng/mL). The OCP levels showed nonnormal distributions and were log-transformed. To evaluate the association between OCPs and related factors such as age, education levels, smoking status, monthly household income, parity, and dietary intake, a Spearman rank correlation was conducted. Multiple linear regression analyses with a stepwise approach were used to assess the effect of potential confounders based on Spearman rank correlation results on OCP levels in cord plasma. Only OCPs with a detection frequency N 50% were analyzed via Spearman rank correlation and multiple linear regression models in our study. All statistical analyses were conducted with SPSS version 22.0 (IBM, New York, NY, USA) for Windows, and two-sided p b 0.05 was considered statistically significant. 3. Results The general characteristics of the selected pregnant women are presented in Table 1. Because of missing demographics and cord blood samples, 972 of the 1000 pregnant women were included in the final statistical analyses. The mean age of the 972 pregnant women who participated in the study was 26.6 ± 0.14 years. Most of the women (90.1%) and their spouses (93.1%) had middle and high school education levels. Most of the women (92.2%) had a length of residency less than 10 years, and the mean length of residency was 4.0 ± 3.8 years. The monthly family household income was subdivided into less than 1000 Yuan (14.2%), between 1000 and 2999 Yuan (23.0%), between 3000 and 4999 Yuan (41.5%), and more than 5000 Yuan (21.3%). Among all subjects, 3 women (0.3%) had a history of smoking, 22 women (2.3%) passively smoked, and 9 women (0.9%) consumed alcoholic beverages during pregnancy. More than half (57.2%) of the pregnant women were primipara, and the mean menarche age of all pregnant women was 13.8 ± 1.3 years. The results of OCP cord blood concentrations are shown in Table 2. The detection frequencies of all analytes were between 0.10% and 100.00%, among which ρ,ρ′-DDE, ρ,ρ′-DDT, aldrin, dieldrin, and methoxychlor had higher detection frequencies of 100.00%, 99.69%, 81.79%, 75.00%, and 74.49%, respectively. Also, ρ,ρ′-DDE, ρ,ρ′-DDT, aldrin, dieldrin, and methoxychlor were the dominant OCPs, with mean levels of 2.01 ± 1.89, 4.31 ± 5.68, 7.29 ± 8.74, 5.27 ± 7.65, and 0.98 ± 1.42 ng/mL, respectively, as well as ρ,ρ′-DDD with the mean concentration of 0.16 ng/mL. Furthermore, among the HCH isomers, β-HCH was predominant in the cord blood, with a mean concentration of 0.68 ng/mL, and the concentrations of α-HCH, γ-HCH, and δ-HCH were 0.21 ng/mL, 0.47 ng/mL, and 0.53 ng/mL, respectively.

Table 1 General characteristics of the pregnant women participating in the study. Characteristics

N

Mean ± S.D. or %

Age (years) Menarche age (years) Education level of the pregnant women None or elementary school Middle and high school College and university or above Education level of their spouses None or elementary school Middle and high school College and university or above Length of residency (years) b10 ≥10 Monthly household income (Yuan) b1000 1000–2999 3000–4999 ≥5000 Smoking history of the pregnant women Yes No Passive smoking of the pregnant women Yes No Alcoholic beverage consumption of the pregnant women Yes No Smoking status of their spouses Yes No Alcohol consumption of their spouses Yes No Parity 1 2 ≥3

972 972

26.6 ± 0.14 13.8 ± 1.3

42 876 54

4.3 90.1 5.6

21 905 46 972 896 76

2.2 93.1 4.7 4.0 ± 3.8 92.2 7.8

138 224 403 207

14.2 23.0 41.5 21.3

3 969

0.3 99.7

22 950

2.3 97.7

9 963

0.9 99.1

395 577

40.6 59.4

910 62

93.6 6.4

556 369 47

57.2 38.0 4.8

Concentrations of ∑OCPs ranged from 12.18 to 486.46 ng/mL (mean 53.13 ± 47.01, median 39.94 ng/mL), while concentrations of ∑Drins ranged from 2.21 to 164.23 ng/mL (mean 13.62 ± 15.04, median

Table 2 Cord blood concentrations of OCPs (ng/mL; n = 972). Analytes

Mean

SD

Median

Range

α-HCH β-HCH γ-HCH δ-HCH ∑HCH ρ,ρ′-DDE ρ,ρ′-DDD ρ,ρ′-DDT ∑DDT Aldrin Dieldrin Endrin Endrin- aldehyde ∑Drins Heptachlor Heptachlor epoxide ∑Heptachlor EndosulfanI EndosulfanII Endosulfan sulfate ∑Endosulfan Methoxychlor ∑OCPs

0.21 0.68 0.47 0.53 1.90 2.01 0.16 4.31 6.48 7.29 5.27 0.45 0.61 13.62 1.50 0.08 1.58 1.73 0.50 0.27 2.50 0.98 53.13

0.42 0.95 4.93 0.69 5.17 1.89 0.38 5.68 6.83 8.74 7.65 0.60 0.10 15.04 2.04 0.13 2.05 5.00 0.38 0.39 5.05 1.42 47.01

bLOD bLOD bLOD bLOD 1.18 1.50 bLOD 2.50 4.40 4.63 3.04 bLOD bLOD 9.07 bLOD bLOD 1.11 bLOD bLOD bLOD 1.78 1.00 39.94

ND to 7.62 ND to 8.95 ND to 153.49 ND to 6.89 0.77 to 155.85 ND to 29.78 ND to 6.76 ND to 60.81 0.21 to 79.46 ND to 76.63 ND to 88.60 ND to 9.37 ND to 3.80 2.21 to 164.23 ND to 48.38 ND to 3.71 1.11 to 48.46 ND to 110.85 ND to 12.12 ND to 4.44 1.78 to 111.47 ND to 33.75 12.18 to 486.46

SD: standard deviation. ND: not detection. LOD: limit of detection.

Frequency (%) 3.70 34.88 4.84 40.84 99.69 10.29 100.00 81.79 75.00 2.78 0.10 14.51 0.93 3.91 0.41 19.75 74.49

D. Luo et al. / Environment International 92–93 (2016) 276–283

9.07 ng/mL), which were greater than ∑ DDT (0.21 to 79.46, mean 6.48 ± 6.83, median 4.40 ng/mL), ∑ Endosulfan (1.78 to 111.47, mean 2.50 ± 5.05, median 1.78 ng/mL), ∑HCH (0.77 to 155.85, mean 1.90 ± 5.17, median 1.18 ng/mL), ∑Heptachlor (1.11 to 48.46, mean 1.58 ± 2.05, median 1.11 ng/mL), and methoxychlor (ND to 33.75, mean 0.98 ± 1.42, median 1.00 ng/mL) in this study. Particularly, the ratios of ρ,ρ′-DDE/ρ,ρ′-DDT, (ρ,ρ′-DDE + ρ,ρ′-DDD)/∑ρ,ρ′-DDT, and αHCH/γ-HCH were 0.47, 0.33, and 0.45, respectively. Compared with concentrations previously reported in cord blood samples of other countries or cities (Table 3), the mean concentration of β-HCH in this study was 8 times lower than that of Veracruz, and 10 times lower than that of Delhi. The current exposure level of βHCH was even higher than that of Catalonia, a specific area in which an organochlorine compound factory was located, while it was comparable with the exposure levels of Shanghai and Russia. The mean concentration of ρ,ρ′-DDE in our study was higher than that of Catalonia, Antwerp, Quebec, Saudi Arabia, Veracruz and Russia, but lower than that of Shanghai, Delhi and Granada. The level of ρ,ρ′-DDT was much higher than that of Shanghai, Catalonia, Delhi, Saudi Arabia, and Veracruz, and lower than that of Granada in previous studies. The levels of both aldrin and dieldrin were significantly higher than that of Shanghai and Delhi, and the level of methoxychlor was higher than that of Shanghai and lower than that of Granada. Table 4 shows the associations among ρ,ρ′-DDE, ρ,ρ′-DDT, aldrin, dieldrin, and methoxychlor in cord blood. There were significant Spearman rank correlation coefficients (p b 0.01) in cord blood among the dominant OCPs. The associations between the levels of major OCPs, general characteristics, and dietary intake habits are shown in Table 5. According to the results of the Spearman rank correlation, we found statistically significant but weak correlations between the levels of major OCPs, general characteristics, and dietary intake habits, with the absolute value of the correlation coefficients ranging from 0.063 to 0.140. The cord blood concentration of ρ,ρ′-DDE was significantly associated with the education level of the pregnant women and their spouses (rs = 0.108, rs = 0.080, respectively), length of residency (rs = − 0.068), parity (rs = − 0.137), poultry (rs = − 0.063), and fish (rs = 0.069). The level of ρ,ρ′-DDT was correlated with the education level of the pregnant women (rs = 0.069), red meat (rs = 0.107), fruit (rs = 0.066), bean products (rs = 0.131), eggs (rs = 0.093), tubers (rs = 0.116), vegetables (rs = 0.067), and tea (rs = 0.065), with statistically significant differences. The Spearman rank correlation coefficients of aldrin levels were 0.113 for the education level of the pregnant women, 0.098 for monthly household income, 0.068 for the education level of their spouses, − 0.085 for poultry, 0.067 for fish, 0.081 for vegetables, and − 0.087 for pickles, while the level of dieldrin in cord blood was only positively associated with the education level of the pregnant women (rs = 0.113). The concentration of methoxychlor was significantly correlated with age (rs = − 0.072), monthly household income (rs = 0.068), red meat (rs = 0.140), fish (rs = 0.100), bean products (rs =

279

Table 4 The results of Spearman rank correlation analyses: associations among ρ,ρ′-DDE, ρ,ρ′-DDT, aldrin, dieldrin and methoxychlor.

ρ,ρ′-DDE ρ,ρ′-DDT Aldrin Dieldrin Methoxychlor

ρ,ρ′-DDE

ρ,ρ′-DDT

Aldrin

Dieldrin

Methoxychlor

1.000 0.408⁎⁎ 0.620⁎⁎ 0.268⁎⁎ 0.229⁎⁎

1.000 0.570⁎⁎ 0.391⁎⁎ 0.232⁎⁎

1.000 0.488⁎⁎ 0.264⁎⁎

1.000 0.121⁎⁎

1.000

⁎⁎ p b 0.01.

0.095), milk (rs = 0.070), eggs (rs = 0.106), tubers (rs = 0.076), and vegetables (rs = 0.072). The multiple linear regression analyses results of ρ,ρ′-DDE, ρ,ρ′-DDT, aldrin, dieldrin, and methoxychlor are depicted in Table 6. The concentration of ρ,ρ′-DDE in cord blood was significantly and positively correlated with fish consumption (β = 0.015) and education level of the pregnant women (β = 0.025), while the association between ρ,ρ′DDE level and parity was negative (β = −0.038). The cord blood ρ,ρ′DDT level was significantly and positively correlated with bean products (β = 0.038) and red meat (β = 0.053), and education level of the pregnant women (β = 0.078) and red meat (β = 0.116) were important contributors to cord blood dieldrin and methoxychlor concentrations, respectively. Aldrin levels were correlated significantly and positively with the education level of the pregnant women (β = 0.060) and monthly household income (β = 0.030), and negatively with poultry (β = −0.048) and pickles (β = −0.045). 4. Discussion Based on the measured concentrations and detection frequencies, ρ,ρ′-DDE, ρ,ρ′-DDT, aldrin, dieldrin, and methoxychlor were the most dominant compounds, with mean concentrations of 2.01 ± 1.89, 4.31 ± 5.68, 7.29 ± 8.74, 5.27 ± 7.65, and 0.98 ± 1.42 ng/mL, respectively, and detection frequencies ranging from 74.49% to 100.00% among the 17 OCPs from the 999 pregnant women in this study. The ratios of ρ,ρ′DDE/ρ,ρ′-DDT and (ρ,ρ′-DDE + ρ,ρ′-DDD)/∑ρ,ρ′-DDT were 0.47 and 0.33, respectively. Actually, the composition of OCPs and their metabolites could provide information regarding contamination sources, input history to the environment, and possible degradation pathways. Generally, technical DDT contains 75% ρ,ρ′-DDT, 15% o,ρ′-DDT, 5% ρ,ρ′-DDE, and b5% other. Since ρ,ρ′-DDE was a metabolite of ρ,ρ′-DDT, the ratio of ρ,ρ′DDE/ρ,ρ′-DDT had been suggested as an indicator of recent and past use of DDT, with the ρ,ρ′-DDE/ρ,ρ′-DDT ratio less than 1 indicating recent input of DDTs (Barakat et al., 2013; Wang et al., 2013). Furthermore, the ratio of (ρ,ρ′-DDE + ρ,ρ′-DDD)/∑ρ,ρ′-DDT less than 0.5 suggested recent input, while those higher than 0.5 implied a historical origin of DDT (Barakat et al., 2013). In this study, the ratios of ρ,ρ′-DDE/ρ,ρ′-DDT and (ρ,ρ′-DDE + ρ,ρ′-DDD)/∑ρ,ρ′-DDT were less than 1 and 0.5, respectively, indicating that the DDTs observed in our study area were considered as a

Table 3 Comparison of OCP mean levels (ng/ml) in cord blood of different countries or cities. Countries or cities

Year

β-HCH

ρ,ρ′-DDE

ρ,ρ′-DDT

Aldrin

Dieldrin

Methoxychlor

References

Shanghai Catalonia Antwerp Delhi Quebec Saudi Arabia Delhi Veracruz Granada Russia Huaihe River

2008–2009 1997–1999 2002–2004 2006–2007 1993–1995 2005–2006 2008–2009 2009 2000–2002 2001–2002 2013–2015

0.68 0.26 NA 7.23 ± 4.24 NA NA NA 5.5 ± 1.6 NA 0.80 ± 1.40 0.68 ± 0.95

2.64 0.83 0.37 3.08 ± 2.72 0.412 0.197 ± 0.961 NA 1.3 ± 0.2 3.62 ± 3.37 0.89 ± 1.08 2.01 ± 1.89

0.25 0.05 NA 1.03 ± 2.63 NA 0.005 ± 0.093 NA 1.1 ± 0.5 5.37 ± 6.55 NA 4.31 ± 5.68

0.14 NA NA NA NA NA 2.41 ± 0.93 NA NA NA 7.29 ± 8.74

0.1362 NA NA NA NA NA 1.39 ± 1.61 NA NA NA 5.27 ± 7.65

0.0259 NA NA NA NA NA NA NA 3.32 ± 4.01 NA 0.98 ± 1.42

Cao et al. (2011) Sala et al. (2001) Maervoet et al. (2007) Pathak et al. (2008) Rhainds et al. (1999) Al-Saleh et al. (2012) Mustafa et al. (2010) Herrero-Mercado et al. (2010) Mariscal-Arcas et al. (2010) Anda et al. (2007) Present study

NA: data are not available

280

D. Luo et al. / Environment International 92–93 (2016) 276–283

Table 5 Correlation coefficients of selected OCPs, general characteristics, and dietary intake habits. ρ,ρ′-DDE

Variables

Age Education level of the pregnant women Length of residency Monthly household income Smoking history of the pregnant women Passive smoking of the pregnant women Alcoholic beverage consumption of the pregnant women Menarche age Parity Education level of their spouses Smoking status of their spouses Alcohol consumption of their spouses Staple food (rice, steamed bread, noodle, corn) Red meat (pork, beef, lamb) Poultry (chicken, duck, goose) Fish Seafood (shrimp, shellfish, sea cucumbers, crab) Fruit Bean product Milk Yogurt Eggs Dry fruits Tubers (potato, sweet potato) Vegetables Pickles Tea

ρ,ρ′-DDT

Aldrin

Dieldrin

Methoxychlor

rs

p

rs

p

rs

p

rs

p

rs

p

0.021 0.108 −0.068 0.057 0.036 −0.021 0.010 0.050 −0.137 0.080 −0.027 −0.024 0.018 0.018 −0.063 0.069 −0.014 0.039 0.028 0.009 −0.021 0.032 0.007 0.017 0.015 −0.036 0.006

0.511 0.001 0.034 0.074 0.261 0.504 0.764 0.116 b0.0001 0.012 0.407 0.461 0.577 0.566 0.050 0.032 0.666 0.228 0.389 0.776 0.516 0.324 0.815 0.605 0.639 0.259 0.861

0.029 0.069 0.019 0.008 −0.007 0.037 −0.011 0.026 0.039 0.047 −0.019 −0.003 0.019 0.107 −0.011 0.059 −0.031 0.066 0.131 0.042 0.028 0.093 0.033 0.116 0.067 −0.056 0.065

0.374 0.032 0.562 0.811 0.834 0.249 0.731 0.427 0.224 0.147 0.546 0.930 0.556 0.001 0.723 0.067 0.331 0.040 b0.0001 0.194 0.385 0.004 0.297 b0.0001 0.038 0.082 0.042

0.046 0.113 0.030 0.098 0.035 −0.038 0.057 0.038 −0.006 0.068 −0.040 −0.016 0.023 0.037 −0.085 0.067 −0.016 0.050 0.030 0.057 0.000 0.055 −0.003 0.045 0.081 −0.087 −0.010

0.151 b0.0001 0.352 0.002 0.274 0.235 0.078 0.234 0.842 0.033 0.213 0.627 0.465 0.246 0.008 0.037 0.613 0.117 0.350 0.078 0.992 0.087 0.931 0.161 0.012 0.007 0.746

0.001 0.113 −0.032 0.013 0.023 −0.017 0.010 0.009 −0.020 0.044 0.045 0.029 0.035 0.020 −0.010 0.021 0.029 −0.019 −0.002 0.008 −0.010 0.022 0.006 0.004 0.020 0.003 0.017

0.970 b0.0001 0.326 0.680 0.473 0.606 0.750 0.776 0.535 0.173 0.162 0.360 0.273 0.534 0.767 0.523 0.358 0.559 0.951 0.815 0.750 0.489 0.859 0.899 0.538 0.925 0.597

−0.072 0.012 −0.032 0.068 0.045 −0.050 0.015 −0.042 −0.023 0.012 −0.042 −0.041 0.024 0.140 0.013 0.100 0.047 0.027 0.095 0.070 −0.035 0.106 0.014 0.076 0.072 −0.040 0.000

0.025 0.708 0.324 0.034 0.162 0.120 0.634 0.187 0.466 0.698 0.187 0.203 0.448 b0.0001 0.693 0.002 0.143 0.406 0.003 0.029 0.276 0.001 0.670 0.018 0.024 0.208 1.000

Bold value: p b 0.05, and p values are 2-tailed.

recent input in the Huaihe River Basin. In view of the ban of DDTs for agricultural use for more than 30 years, the possible sources of DDTs might be mainly the manufacturing process for dicofol and anti-fouling paint, as well as malaria controlling in medicine. The mean concentration order of the isomers of HCHs was β-HCH (0.68 ng/mL) N δ-HCH (0.53 ng/mL) N γ-HCH (0.47 ng/mL) N α-HCH

(0.21 ng/mL), and the ratio of α-HCH/γ-HCH was 0.45. The technical mixtures of HCHs typically contained 60%–70% α, 5%–12% β, 10%–12% γ, 6%–10% δ, 3%–4% ε, in which γ-HCH was the isomer with the highest pesticidal activity, while lindane as an insecticide contained approximately 99% γ-HCH (Willett et al., 1998). Consequently, the ratio of αHCH/γ-HCH could indicate the contamination sources of HCHs to

Table 6 Multiple linear regression analyses of log ρ,ρ′-DDE, log ρ,ρ′-DDT, log aldrin, log dieldrin, and log methoxychlor. Unstandardized coefficients

Standardized coefficients

β

Std. error

β

0.135 −0.038 0.015 0.025

0.059 0.014 0.007 0.013

−0.088 0.072 0.064

2.288 −2.762 2.250 1.987

0.248 0.038 0.053

0.044 0.014 0.020

0.089 0.087

log aldrinc (Constant) Education level of the pregnant women Monthly household income Poultry Pickles

0.271 0.060 0.030 −0.048 −0.045

0.102 0.023 0.009 0.014 0.019

log dieldrind (Constant) Education level of the pregnant women

0.098 0.078 −0.555 0.116

log ρ,ρ′-DDEa (Constant) Parity Fish Education level of the pregnant women log ρ,ρ′-DDTb (Constant) Bean product Red meat

log methoxychlore (Constant) Red meat a b c d e

t

Sig.

95% Confidence interval for β Lower bound

Upper bound

0.022 0.006 0.025 0.047

0.019 −0.065 0.002 0.000

0.250 −0.011 0.028 0.049

5.568 2.688 2.629

0.000 0.007 0.009

0.160 0.010 0.013

0.335 0.066 0.092

0.085 0.111 −0.114 −0.075

2.650 2.654 3.342 −3.463 −2.374

0.008 0.008 0.001 0.001 0.018

0.070 0.016 0.012 −0.075 −0.083

0.471 0.105 0.047 −0.021 −0.008

0.104 0.025

0.100

0.941 3.145

0.347 0.002

−0.107 0.030

0.303 0.127

0.064 0.029

0.126

−8.660 3.954

0.000 0.000

−0.681 0.059

−0.429 0.174

Variables introduced into the model included: education level of the pregnant women, length of residency, parity, education level of their spouse, poultry, fish. Variables introduced into the model included: education level of the pregnant women, red meat, fruit, bean products, eggs, tubers, vegetables, tea. Variables introduced into the model included: education level of the pregnant women, monthly household income, education level of their spouse, poultry, seafood, vegetables, pickle. Variables introduced into the model included: education level of the pregnant women. Variables introduced into the model included: age, monthly household income, red meat, fish, bean products, milk, eggs, tubers, vegetables.

D. Luo et al. / Environment International 92–93 (2016) 276–283

some extent. It was suggested that if α-HCH/γ-HCH was less than 1, the possible source was lindane, while 3 b α-HCH/γ-HCH b 7 indicated a technical source (Qiao et al., 2010). In our findings, the ratio of αHCH/γ-HCH was less than 1, thus recent input of lindane was supposed to be the possible source. In addition, due to the low water solubility, vapor pressure, and long half-life, β-HCH was generally considered the most persistent in the environment and most resistant to biodegradation compared with other isomers (Li et al., 2014; Yang et al., 2005). Meanwhile, we should also note that γ-HCH and α-HCH could be transformed into β-HCH (Barakat et al., 2013). The predominance of the occurrence of β-HCH in this study confirmed these findings, suggesting that HCH residue was derived mainly from historical use of technical HCH in this region. China experienced large-scale production and consumption of OCPs from the 1950s to 1980s, mainly DDTs and HCHs. However, aldrin and dieldrin had never been produced at a large scale in China (only for research or trial production). Additionally, due to their persistence, bioaccumulation, high toxicity, semi-volatility, and long-range transport, the ban of OCPs, including DDTs, HCHs, aldrin, and dieldrin, had been performed since the 1980s in many countries including China. According to the Stockholm Convention on POPs by the United Nations Environment Programme (UNEP) in 2004, 12 “dirty” substances were first listed as POPs, among which 9 were OCPs: aldrin, endrin, dieldrin, heptachlor, chlordane, mirex, toxaphene, DDT, and HCB (Zhang et al., 2012). The Huaihe River Basin, located in North China, had been well known for agricultural production, and a large quantity of OCPs had been consumed in this region. Previous studies to investigate the contamination status of OCPs in this area were few, and most of the available data focused only on HCHs and DDTs in environment media, with relatively low levels of aldrin and dieldrin (Feng et al., 2011; Liu et al., 2015; Meng et al., 2014; Sun et al., 2010). To our knowledge, aldrin and dieldrin that had strong insecticidal properties could be used for crop protection with lower persistence compared with DDT, and aldrin could rapidly be converted to dieldrin. As a result of the lower toxicity and persistence compared with DDT, methoxychlor was applied in agriculture as an alternative insecticide to DDT. Therefore, it could be hypothesized that there recently were emissions of aldrin and dieldrin in the Huaihe River Basin based on the higher frequencies and exposure levels of aldrin and dieldrin, as well as methoxychlor. However, usage information about OCPs, especially aldrin, dieldrin, and methoxychlor, in this region was lacking. Additionally, long-range transport was also another inevitable route for OCP contamination in China (Zhang et al., 2012). Further studies are needed to better understand the contamination status of currently detected OCPs. In comparison with studies performed in other countries or cities, we found that concentrations of ρ,ρ′-DDT, aldrin, dieldrin, and methoxychlor in cord blood were significantly higher than those observed in Shanghai. Also, the mean levels of ρ,ρ′-DDE and ρ,ρ′-DDT were significantly higher than those from developed and developing countries or cities, such as Catalonia (in Spain), Antwerp (in Belgium), Quebec (in Canada), Granada (in Spain), Saudi Arabia, Delhi (in India), Veracruz (in Mexico) and Russia. The results of our study demonstrate significant associations among the major OCPs in cord blood, which could imply to a certain extent that some OCPs might share similar exposure pathways, especially dietary intakes, although other environmental sources of exposure might also play a role. Since no participant in our study reported to have a history of occupational exposure to OCPs, the most possible sources of OCP exposure were dietary intake and lifestyle-related factors. The result of the multiple linear regression model of ρ,ρ′-DDE shows a negative association between cord blood OCP levels and parity, especially ρ,ρ′-DDE level and parity (p b 0.0001), which was in accordance with the outcome of a previous report (Cao et al., 2011). Based on the findings by Lee et al. (2007), the negative association might be ascribed to breastfeeding history (Lee et al., 2007). The pregnant women with a higher monthly household income tended to have significantly higher

281

cord blood concentrations of aldrin in our study. Moreover, we found that the education level of the pregnant women was one of the most important contributors to ρ,ρ′-DDE, aldrin, and dieldrin concentrations in cord blood, based on multiple linear regression analyses. Some of these results were in line with results from a Shanghai study previously conducted by Cao et al. (2011). The OCP residues in foodstuff had been investigated by Nakata et al. (2002), and relatively high DDTs were found in meat. People who had a higher monthly household income and education level were more likely to consume foodstuff containing high nutritional value and paid more attention to the quality of meat. As a consequence of the high lipophilicity and biological accumulation, OCP residues in foodstuff, especially in meat, could be transported into the human body via the food chain and the food web. Several previous studies examined the association between dietary intake and OCP concentrations in blood, with results to indicate that dietary intake might be a crucial contributor to OCP exposure levels in the human body (Cao et al., 2011; Devoto et al., 1998; Hanaoka et al., 2002; Lee et al., 2007; Mariscal-Arcas et al., 2010). ρ,ρ′-DDT and methoxychlor concentrations in cord blood were significantly and positively correlated with red meat, including pork, beef, and lamb, in multiple linear regression analyses, which was consistent with reported results carried out by other research groups (Cao et al., 2011; Devoto et al., 1998; Lee et al., 2007). Additionally, a negative association existed between cord blood OCP levels and the consumption of poultry in our study, which did not correspond to the study conducted by Cao et al. (2011). In addition, a clear link had been found between the levels of organochlorines in the blood and fish intake in different studies (Glynn et al., 2007; Hanaoka et al., 2002; Wang et al., 2013). The association was further confirmed by our finding of a significantly positive correlation between ρ,ρ′-DDE level and fish consumption, indicating that fish intake was one of the important contributing factors in cord blood ρ,ρ′-DDE level. Similar to the results of Lee et al. (2007) and Hanaoka et al. (2002), the cord blood ρ,ρ′-DDT level was significantly and positively correlated with bean product intake in our study (Hanaoka et al., 2002; Lee et al., 2007). With regard to the finding of a negative correlation between pickle intake and aldrin levels, it could be assumed that an increasing number of people had discovered the potentially inverse impact of pickle intake on human health. Nakata et al. (2002) conducted a study to investigate the residue levels of organochlorine compounds, including DDTs and HCHs, in foodstuff in China from 2000 to 2001, and suggested a high detection rate (85%) and concentration (34,000 ng/g lipid weight) of DDTs in Shanghai, although a virtual ban of OCPs had been put into effect in China since the 1980s. Zhou et al. (2012) investigated dietary exposure to OCPs in Chinese populations using the total diet study approach in 2007, and the occurrence frequencies were 39%, 13%, 37%, and 5% for DDT and its metabolites, HCH, chlordane, and heptachlor, respectively, in food samples, including cereals, legumes, nuts, potatoes, meat, eggs, milk, vegetables, and fruits. The exposure route of OCPs in healthy pregnant women was mainly derived from the ingestion of contaminated food, and the existence of OCPs in these types of foods might explain our results to some extent. 5. Conclusion This study is the first detailed report of OCP levels in cord blood from 999 pregnant women in the Huaihe River Basin of China, among which ρ,ρ′-DDE, ρ,ρ′-DDT, aldrin, dieldrin, and methoxychlor were the most dominant compounds, with higher measured concentrations and detection frequencies. In this study, it was found that higher levels of DDTs, aldrin, dieldrin, and methoxychlor observed in our study area were considered recent input. Most of the HCHs in cord blood were derived not only from historical use of technical HCH, but also from additional use of lindane. Similar to other studies, the education level of the pregnant women and monthly household income were observed to have a positive correlation with OCP levels, particularly ρ,ρ′-DDE, aldrin, and

282

D. Luo et al. / Environment International 92–93 (2016) 276–283

dieldrin. Furthermore, the results indicated that the consumption of red meat, fish, and bean products might be important contributing factors to increased OCP concentrations in cord blood, while the intake of poultry and pickles were negatively correlated with aldrin levels. In consideration of potential health effects of human exposure to OCPs, biomonitoring studies and investigations on OCPs levels in the human body and food are necessary to further confirm these findings, as well as to evaluate the potential health risks of OCPs among individuals. Conflict of interest The authors have no conflict of interest to declare. Acknowledgements The authors want to thank participators who volunteered to participate in this study and permit the collection of umbilical cord blood, as well as medical staff who provide technical assistance and dietary intake survey. This research was supported by the Key Projects in the National Science and Technology Pillar Program in the Twelveth Five-year Plan Period of China (2013BAI12B03), the Fundamental Research Funds for the Central Universities (HUST: 2015MS084), and the Natural Science Foundation of China (21577043). References Al-Saleh, I., Al-Doush, I., Alsabbaheen, A., Mohamed, G.E.D., et al., 2012. Levels of DDT and its metabolites in placenta, maternal and cord blood and their potential influence on neonatal anthropometric measures. Sci. Total Environ. 416, 62–74. Anda, E.E., Nieboer, E., Dudarev, A., Sandanger, T., et al., 2007. Intra-and intercompartmental associations between levels of organochlorines in maternal plasma, cord plasma and breast milk, and lead and cadmium in whole blood, for indigenous peoples of Chukotka, Russia. J. Environ. Monit. 9, 884–893. Barakat, A.O., Khairy, M., Aukaily, I., 2013. Persistent organochlorine pesticide and PCB residues in surface sediments of Lake Qarun, a protected area of Egypt. Chemosphere 90, 2467–2476. Bretveld, R.W., Thomas, C., Scheepers, P., Zielhuis, G.A., et al., 2006. Pesticide exposure: the hormonal function of the female reproductive system disrupted. Reprod. Biol. Endocrinol. 4, 30. Cao, L.-L., Yan, C.-H., Yu, X.-D., Tian, Y., et al., 2011. Relationship between serum concentrations of polychlorinated biphenyls and organochlorine pesticides and dietary habits of pregnant women in Shanghai. Sci. Total Environ. 409, 2997–3002. Clarkson, T.W., 1995. Environmental contaminants in the food chain. Am. J. Clin. Nutr. 61, 682S–686S. Devoto, E., Kohlmeier, L., Heeschen, W., 1998. Some dietary predictors of plasma organochlorine concentrations in an elderly German population. Arch. Environ. Health 53, 147–155. Dewan, P., Jain, V., Gupta, P., Banerjee, B.D., 2013. Organochlorine pesticide residues in maternal blood, cord blood, placenta, and breastmilk and their relation to birth size. Chemosphere 90, 1704–1710. Eggesbø, M., Stigum, H., Longnecker, M.P., Polder, A., et al., 2009. Levels of hexachlorobenzene (HCB) in breast milk in relation to birth weight in a Norwegian cohort. Environ. Res. 109, 559–566. Eskenazi, B., Harley, K., Bradman, A., Weltzien, E., et al., 2004. Association of in utero organophosphate pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ. Health Perspect. 112, 1116. Eskenazi, B., Marks, A.R., Bradman, A., Fenster, L., et al., 2006. In utero exposure to dichlorodiphenyltrichloroethane (DDT) and dichlorodiphenyldichloroethylene (DDE) and neurodevelopment among young Mexican American children. Pediatrics 118, 233–241. Fang, W., Jiang, X., Bian, Y.-r., Yao, F.-x., et al., 2007. Organochlorine pesticides in soils under different land usage in the Taihu Lake region, China. J. Environ.Sci. China 19, 584–590. Feng, J., Zhai, M., Liu, Q., Sun, J., et al., 2011. Residues of organochlorine pesticides (OCPs) in upper reach of the Huaihe River, East China. Ecotoxicol. Environ. Saf. 74, 2252–2259. Glynn, A., Aune, M., Darnerud, P.O., Cnattingius, S., et al., 2007. Determinants of serum concentrations of organochlorine compounds in Swedish pregnant women: a crosssectional study. Environ. Health 6, 2. Guo, H., Jin, Y., Cheng, Y., Leaderer, B., et al., 2014. Prenatal exposure to organochlorine pesticides and infant birth weight in China. Chemosphere 110, 1–7. Hanaoka, T., Takahashi, Y., Kobayashi, M., Sasaki, S., et al., 2002. Residuals of betahexachlorocyclohexane, dichlorodiphenyltrichloroethane, and hexachlorobenzene in serum, and relations with consumption of dietary components in rural residents in Japan. Sci. Total Environ. 286, 119–127. Herrero-Mercado, M., Waliszewski, S., Caba, M., Martínez-Valenzuela, C., et al., 2010. Organochlorine pesticide levels in umbilical cord blood of newborn in Veracruz, Mexico. Bull. Environ. Contam. Toxicol. 85, 367–371.

Hong, H., Wen-hau, O., Lian-Sheng, W., 2006. Semivolatile organic compounds, organochlorine pesticides and heavy metals in sediments and risk assessment in Huaihe River of China. J. Environ. Sci. 18, 236–241. Kamel, F., Hoppin, J.A., 2004. Association of pesticide exposure with neurologic dysfunction and disease. Environ. Health Perspect. 112, 950–958. Keifer, M.C., Firestone, J., 2007. Neurotoxicity of pesticides. J. Agromed. 12, 17–25. Korrick, S.A., Chen, C., Damokosh, A.I., Ni, J., et al., 2001. Association of DDT with spontaneous abortion: a case-control study. Ann. Epidemiol. 11, 491–496. Lee, S.-A., Dai, Q., Zheng, W., Gao, Y.-T., et al., 2007. Association of serum concentration of organochlorine pesticides with dietary intake and other lifestyle factors among urban Chinese women. Environ. Int. 33, 157-163. Li, J., Li, N., Ma, M., Giesy, J.P., et al., 2008. In vitro profiling of the endocrine disrupting potency of organochlorine pesticides. Toxicol. Lett. 183, 65–71. Li, C., Cheng, Y., Tang, Q., Lin, S., et al., 2014. The association between prenatal exposure to organochlorine pesticides and thyroid hormone levels in newborns in Yancheng, China. Environ. Res. 129, 47–51. Liu, M., Feng, J., Kang, B., Chen, Y., et al., 2015. Ecological and health risks of DDTs and HCHs in surface water from the upper reaches of the Huaihe River. Toxicol. Environ. Chem. 97, 1124–1136. Lopez-Espinosa, M.-J., Murcia, M., Iñiguez, C., Vizcaino, E., et al., 2011. Prenatal exposure to organochlorine compounds and birth size. Pediatrics 128, e127–e134. Maervoet, J., Vermeir, G., Covaci, A., Van Larebeke, N., et al., 2007. Association of thyroid hormone concentrations with levels of organochlorine compounds in cord blood of neonates. Environ. Health Perspect. 115, 1780–1786. Mariscal-Arcas, M., Lopez-Martinez, C., Granada, A., Olea, N., et al., 2010. Organochlorine pesticides in umbilical cord blood serum of women from Southern Spain and adherence to the Mediterranean diet. Food Chem. Toxicol. 48, 1311–1315. McGlynn, K.A., Abnet, C.C., Zhang, M., Sun, X.-D., et al., 2006. Serum concentrations of 1, 1, 1-trichloro-2, 2-bis (p-chlorophenyl) ethane (DDT) and 1, 1-dichloro-2, 2-bis (pchlorophenyl) ethylene (DDE) and risk of primary liver cancer. J. Natl. Cancer Inst. 98, 1005–1010. Meng, J., Wang, T., Wang, P., Giesy, J.P., et al., 2014. Perfluoroalkyl substances and organochlorine pesticides in sediments from Huaihe watershed in China. J. Environ. Sci. 26, 2198–2206. Mustafa, M., Pathak, R., Tripathi, A., Ahmed, R.S., et al., 2010. Maternal and cord blood levels of Aldrin and Dieldrin in Delhi population. Environ. Monit. Assess. 171, 633–638. Nagayama, J., Tsuji, H., Iida, T., Nakagawa, R., et al., 2007. Immunologic effects of perinatal exposure to dioxins, PCBs and organochlorine pesticides in Japanese infants. Chemosphere 67, S393–S398. Nakata, H., Kawazoe, M., Arizono, K., Abe, S., et al., 2002. Organochlorine pesticides and polychlorinated biphenyl residues in foodstuffs and human tissues from China: status of contamination, historical trend, and human dietary exposure. Arch. Environ. Contam. Toxicol. 43, 0473–0480. Nakata, H., Nasu, T., Abe, S.-I., Kitano, T., et al., 2005. Organochlorine contaminants in human adipose tissues from China: mass balance approach for estimating historical Chinese exposure to DDTs. Environ. Sci. Technol. 39, 4714–4720. Nicolopoulou-Stamati, P., Pitsos, M., 2001. The impact of endocrine disrupters on the female reproductive system. Hum. Reprod. Update 7, 323–330. No, T.S., 2005. Stockholm Convention on Persistent Organic Pollutants. Available at: https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/ 273235/6581.pdf. Noakes, P.S., Taylor, P., Wilkinson, S., Prescott, S.L., 2006. The relationship between persistent organic pollutants in maternal and neonatal tissues and immune responses to allergens: a novel exploratory study. Chemosphere 63, 1304–1311. Pathak, R., Suke, S.G., Ahmed, R.S., Tripathi, A., et al., 2008. Endosulfan and other organochlorine pesticide residues in maternal and cord blood in North Indian population. Bull. Environ. Contam. Toxicol. 81, 216–219. Pathak, R., Ahmed, R.S., Tripathi, A., Guleria, K., et al., 2009. Maternal and cord blood levels of organochlorine pesticides: association with preterm labor. Clin. Biochem. 42, 746–749. Poon, B., Leung, C., Wong, C., Wong, M., 2005. Polychlorinated biphenyls and organochlorine pesticides in human adipose tissue and breast milk collected in Hong Kong. Arch. Environ. Contam. Toxicol. 49, 274–282. Qiao, M., An, T., Zeng, X., Zhang, D., et al., 2010. Safety assessment of the source water within the Pearl River Delta on the aspect of organochlorine pesticides contamination. J. Environ. Monit. 12, 1666–1677. Qiu, X., Zhu, T., Li, J., Pan, H., et al., 2004. Organochlorine pesticides in the air around the Taihu Lake, China. Environ. Sci. Technol. 38, 1368–1374. Ren, A., Qiu, X., Jin, L., Ma, J., et al., 2011. Association of selected persistent organic pollutants in the placenta with the risk of neural tube defects. Proc. Natl. Acad. Sci. U.S.A. 108, 12770–12775. Rhainds, M., Levallois, P., Dewailly, É., Ayotte, P., 1999. Lead, mercury, and organochlorine compound levels in cord blood in Quebec, Canada. Arch. Environ. Health 54, 40–47. Safea, S., 2004. Endocrine disruptors and human health: is there a problem. Toxicology 205, 3–10. Sagiv, S.K., Tolbert, P.E., Altshul, L.M., Korrick, S.A., 2007. Organochlorine exposures during pregnancy and infant size at birth. Epidemiology 18, 120–129. Sala, M., Ribas-Fito, N., Cardo, E., De Muga, M., et al., 2001. Levels of hexachlorobenzene and other organochlorine compounds in cord blood: exposure across placenta. Chemosphere 43, 895–901. Saxena, M., Siddiqui, M., Bhargava, A., Krishna Murti, C., et al., 1981a. Placental transfer of pesticides in humans. Arch. Toxicol. 48, 127–134. Saxena, M., Siddiqui, M., Seth, T., Murti, C.K., et al., 1981b. Organochlorine pesticides in specimens from women undergoing spontaneous abortion, premature or full-term delivery. J. Anal. Toxicol. 5, 6–9.

D. Luo et al. / Environment International 92–93 (2016) 276–283 Shen, L., Wania, F., Lei, Y.D., Teixeira, C., et al., 2005. Atmospheric distribution and longrange transport behavior of organochlorine pesticides in North America. Environ. Sci. Technol. 39, 409–420. Sheng, J., Wang, X., Gong, P., Joswiak, D.R., et al., 2013. Monsoon-driven transport of organochlorine pesticides and polychlorinated biphenyls to the Tibetan Plateau: three year atmospheric monitoring study. Environ. Sci. Technol. 47, 3199–3208. Sun, J., Feng, J., Liu, Q., Li, Q., 2010. Distribution and sources of organochlorine pesticides (OCPs) in sediments from upper reach of Huaihe River, East China. J. Hazard. Mater. 184, 141–146. Sundberg, S.E., Ellington, J.J., Evans, J.J., 2006. A simple and fast extraction method for organochlorine pesticides and polychlorinated biphenyls in small volumes of avian serum. J. Chromatogr. B 831, 99–104. Tao, S., Liu, W., Li, X., Zhou, D., et al., 2009. Organochlorine pesticide residuals in chickens and eggs at a poultry farm in Beijing, China. Environ. Pollut. 157, 497–502. Toft, G., Hagmar, L., Giwercman, A., Bonde, J.P., 2004. Epidemiological evidence on reproductive effects of persistent organochlorines in humans. Reprod. Toxicol. 19, 5–26. Wang, B., Yu, G., Yu, Y., Zhang, Z., et al., 2006. Aquatic ecological risk assessment of OCPs in Huaihe River, Jiangsu section. Chin. J. Geochem. 25, 157. Wang, H.-S., Chen, Z.-J., Wei, W., Man, Y.-B., et al., 2013. Concentrations of organochlorine pesticides (OCPs) in human blood plasma from Hong Kong: markers of exposure and sources from fish. Environ. Int. 54, 18–25.

283

Weiderpass, E., Adami, H.-O., Baron, J.A., Wicklund-Glynn, A., et al., 2000. Organochlorines and endometrial cancer risk. Cancer Epidemiol. Biomark. Prev. 9, 487–493. Willett, K.L., Ulrich, E.M., Hites, R.A., 1998. Differential toxicity and environmental fates of hexachlorocyclohexane isomers. Environ. Sci. Technol. 32, 2197–2207. Wolff, M.S., Berkowitz, G.S., Brower, S., Senie, R., et al., 2000. Organochlorine exposures and breast cancer risk in New York City women. Environ. Res. 84, 151–161. Xu, X., Dailey, A.B., Talbott, E.O., Ilacqua, V.A., et al., 2010. Associations of serum concentrations of organochlorine pesticides with breast cancer and prostate cancer in US adults. Environ. Health Perspect. 118, 60–66. Yang, R.-q., Lv, A.-h., Shi, J.-b., Jiang, G.-b., 2005. The levels and distribution of organochlorine pesticides (OCPs) in sediments from the Haihe River, China. Chemosphere 61, 347–354. Yang, N., Matsuda, M., Kawano, M., Wakimoto, T., 2006. PCBs and organochlorine pesticides (OCPs) in edible fish and shellfish from China. Chemosphere 63, 1342–1352. Zhang, A., Fang, L., Wang, J., Liu, W., et al., 2012. Residues of currently and never used organochlorine pesticides in agricultural soils from Zhejiang Province, China. J. Agric. Food. Chem. 60, 2982–2988. Zhou, R., Zhu, L., Yang, K., Chen, Y., 2006. Distribution of organochlorine pesticides in surface water and sediments from Qiantang River, East China. J. Hazard. Mater. 137, 68–75. Zhou, P., Zhao, Y., Li, J., Wu, G., et al., 2012. Dietary exposure to persistent organochlorine pesticides in 2007 Chinese total diet study. Environ. Int. 42, 152–159.